The significance of nitrogen cost minimization in proteomes of marine microorganisms
Identifieur interne : 000028 ( Pmc/Curation ); précédent : 000027; suivant : 000029The significance of nitrogen cost minimization in proteomes of marine microorganisms
Auteurs : Joseph J. Grzymski [États-Unis] ; Alex M. Dussaq [États-Unis]Source :
- The ISME Journal [ 1751-7362 ] ; 2011.
Abstract
Marine microorganisms thrive under low levels of nitrogen (N). N cost minimization is a major selective pressure imprinted on open-ocean microorganism genomes. Here we show that amino-acid sequences from the open ocean are reduced in N, but increased in average mass compared with coastal-ocean microorganisms. Nutrient limitation exerts significant pressure on organisms supporting the trade-off between N cost minimization and increased average mass of amino acids that is a function of increased A+T codon usage. N cost minimization, especially of highly expressed proteins, reduces the total cellular N budget by 2.7–10% this minimization in combination with reduction in genome size and cell size is an evolutionary adaptation to nutrient limitation. The biogeochemical and evolutionary precedent for these findings suggests that N limitation is a stronger selective force in the ocean than biosynthetic costs and is an important evolutionary strategy in resource-limited ecosystems.
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DOI: 10.1038/ismej.2011.72
PubMed: 21697958
PubMed Central: 3246230
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The significance of nitrogen cost minimization in proteomes of marine microorganisms</title><author><name sortKey="Grzymski, Joseph J" sort="Grzymski, Joseph J" uniqKey="Grzymski J" first="Joseph J" last="Grzymski">Joseph J. Grzymski</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Division of Earth and Ecosystem Sciences, Desert Research Institute</institution>, Reno, NV,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Dussaq, Alex M" sort="Dussaq, Alex M" uniqKey="Dussaq A" first="Alex M" last="Dussaq">Alex M. Dussaq</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Division of Earth and Ecosystem Sciences, Desert Research Institute</institution>, Reno, NV,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">21697958</idno><idno type="pmc">3246230</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3246230</idno><idno type="RBID">PMC:3246230</idno><idno type="doi">10.1038/ismej.2011.72</idno><date when="2011">2011</date><idno type="wicri:Area/Pmc/Corpus">000028</idno><idno type="wicri:Area/Pmc/Curation">000028</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The significance of nitrogen cost minimization in proteomes of marine microorganisms</title><author><name sortKey="Grzymski, Joseph J" sort="Grzymski, Joseph J" uniqKey="Grzymski J" first="Joseph J" last="Grzymski">Joseph J. Grzymski</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Division of Earth and Ecosystem Sciences, Desert Research Institute</institution>, Reno, NV,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Dussaq, Alex M" sort="Dussaq, Alex M" uniqKey="Dussaq A" first="Alex M" last="Dussaq">Alex M. Dussaq</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Division of Earth and Ecosystem Sciences, Desert Research Institute</institution>, Reno, NV,<country>USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">The ISME Journal</title><idno type="ISSN">1751-7362</idno><idno type="eISSN">1751-7370</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Marine microorganisms thrive under low levels of nitrogen (N). N cost minimization is a major selective pressure imprinted on open-ocean microorganism genomes. Here we show that amino-acid sequences from the open ocean are reduced in N, but increased in average mass compared with coastal-ocean microorganisms. Nutrient limitation exerts significant pressure on organisms supporting the trade-off between N cost minimization and increased average mass of amino acids that is a function of increased A+T codon usage. N cost minimization, especially of highly expressed proteins, reduces the total cellular N budget by 2.7–10% this minimization in combination with reduction in genome size and cell size is an evolutionary adaptation to nutrient limitation. The biogeochemical and evolutionary precedent for these findings suggests that N limitation is a stronger selective force in the ocean than biosynthetic costs and is an important evolutionary strategy in resource-limited ecosystems.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Akashi, H" uniqKey="Akashi H">H Akashi</name></author><author><name sortKey="Gojobori, T" uniqKey="Gojobori T">T Gojobori</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Barrai, I" uniqKey="Barrai I">I Barrai</name></author><author><name sortKey="Volinia, S" uniqKey="Volinia S">S Volinia</name></author><author><name sortKey="Scapoli, C" uniqKey="Scapoli C">C Scapoli</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Baudouin Cornu, P" uniqKey="Baudouin Cornu P">P Baudouin-Cornu</name></author><author><name sortKey="Schuerer, K" uniqKey="Schuerer K">K Schuerer</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">ISME J</journal-id><journal-title-group><journal-title>The ISME Journal</journal-title></journal-title-group><issn pub-type="ppub">1751-7362</issn><issn pub-type="epub">1751-7370</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">21697958</article-id><article-id pub-id-type="pmc">3246230</article-id><article-id pub-id-type="pii">ismej201172</article-id><article-id pub-id-type="doi">10.1038/ismej.2011.72</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject></subj-group></article-categories><title-group><article-title>The significance of nitrogen cost minimization in proteomes of marine microorganisms</article-title><alt-title alt-title-type="running">Nitrogen cost minimization in marine microbes</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Grzymski</surname><given-names>Joseph J</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="corresp" rid="caf1">*</xref></contrib><contrib contrib-type="author"><name><surname>Dussaq</surname><given-names>Alex M</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><aff id="aff1"><label>1</label><institution>Division of Earth and Ecosystem Sciences, Desert Research Institute</institution>, Reno, NV,<country>USA</country></aff></contrib-group><author-notes><corresp id="caf1"><label>*</label><institution>Division of Earth and Ecosystem Studies, Desert Research Institute</institution>, 2215 Raggio Parkway, Reno, NV 89512, <country>USA</country>. E-mail: <email>joeg@dri.edu</email></corresp></author-notes><pub-date pub-type="ppub"><month>01</month><year>2012</year></pub-date><pub-date pub-type="epub"><day>23</day><month>06</month><year>2011</year></pub-date><pub-date pub-type="pmc-release"><day>1</day><month>1</month><year>2012</year></pub-date><volume>6</volume><issue>1</issue><fpage>71</fpage><lpage>80</lpage><history><date date-type="received"><day>25</day><month>01</month><year>2011</year></date><date date-type="rev-recd"><day>30</day><month>03</month><year>2011</year></date><date date-type="accepted"><day>26</day><month>04</month><year>2011</year></date></history><permissions><copyright-statement>Copyright © 2012 International Society for Microbial Ecology</copyright-statement><copyright-year>2012</copyright-year><copyright-holder>International Society for Microbial Ecology</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under the Creative Commons Attribution-NonCommercial-No Derivative Works 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/</license-p></license></permissions><abstract><p>Marine microorganisms thrive under low levels of nitrogen (N). N cost minimization is a major selective pressure imprinted on open-ocean microorganism genomes. Here we show that amino-acid sequences from the open ocean are reduced in N, but increased in average mass compared with coastal-ocean microorganisms. Nutrient limitation exerts significant pressure on organisms supporting the trade-off between N cost minimization and increased average mass of amino acids that is a function of increased A+T codon usage. N cost minimization, especially of highly expressed proteins, reduces the total cellular N budget by 2.7–10% this minimization in combination with reduction in genome size and cell size is an evolutionary adaptation to nutrient limitation. The biogeochemical and evolutionary precedent for these findings suggests that N limitation is a stronger selective force in the ocean than biosynthetic costs and is an important evolutionary strategy in resource-limited ecosystems.</p></abstract><kwd-group><kwd>amino-acid usage</kwd><kwd>cost minimization</kwd><kwd>oligotrophy</kwd><kwd>nitrogen</kwd><kwd>resource limitation</kwd></kwd-group></article-meta></front><floats-group><fig id="fig1"><label>Figure 1</label><caption><p>Annual 10 m nitrate concentration for world oceans. Red dots are GOS sampling sites used in our analyses.</p></caption><graphic xlink:href="ismej201172f1"></graphic></fig><fig id="fig2"><label>Figure 2</label><caption><p>Nitrogens per amino-acid residue side chain for GOS environmental genome data. (<bold>a</bold>) Quantile plots of the average number of nitrogen ARSC for GOS stations. Red lines represent coastal-ocean sites from the GOS data set as defined in Materials and methods. Blue lines are from open-ocean sites. (<bold>b</bold>) The median N ARSC for each GOS site and one from a sewage metagenome. The color reproduction of this figure is available at the <italic>ISME Journal</italic> online.</p></caption><graphic xlink:href="ismej201172f2"></graphic></fig><fig id="fig3"><label>Figure 3</label><caption><p>Median nitrogen ARSC as it correlates to proximity of landmass. The correlation between the nearest land mass and median N ARSC for each GOS metagenome station. Spearman correlation coefficients are presented in <xref ref-type="supplementary-material" rid="sup1">Supplementary Table S1</xref>.</p></caption><graphic xlink:href="ismej201172f3"></graphic></fig><fig id="fig4"><label>Figure 4</label><caption><p>Circular genome plots of <italic>Prochlorococcus marinus</italic> ecotypes. (<bold>a</bold>) Coding (gray) and non-coding regions (red=leading strand, blue=lagging strand) for the <italic>P. marinus</italic> ecotype MIT 9313. Additional data are available in <xref ref-type="supplementary-material" rid="sup1">Supplementary Tables S4 and S5c</xref>. Averaged nitrogen ARSC for each ORF is plotted as a colored bar graph, with green indicating high nitrogen ARSC and red indicating lower as in Materials and methods. The concentric rings scale represents an increase of 0.03 N ARSC. (<bold>b</bold>) As in (<bold>a</bold>), but for the <italic>P. marinus</italic> ecotype CCMP 1986. (<bold>c</bold>) As in <bold>a</bold>, but bar graphs represent subtraction of strain MIT9313—CCMP1986 N ARSC values for all genes in the core genome (1286) excluding hypothetical proteins. Green indicates positive values and red indicates negative values. The concentric rings scale represents changes of 0.03 N ARSC. (<bold>d</bold>) Same as <bold>c</bold> except representing the average amino-acid mass difference for strain MIT9313—CCMP1986. The concentric rings scale represents changes of 3 g mol<sup>−1</sup>.</p></caption><graphic xlink:href="ismej201172f4"></graphic></fig><table-wrap id="tbl1"><label>Table 1</label><caption><title>Protein requirements in theoretical marine microorganism populations determined by modeling</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="±"></col><col align="char" char="±"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><italic>Description</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>Cell size (μm<sup>3</sup>)</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>Genome size (Mb)</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>G+C (%)</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>Total protein mass (fg cell</italic><sup><italic>−1</italic></sup><italic>)</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>N ARSC</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>Average mass (g mol</italic><sup><italic>−1</italic></sup><italic>)</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>Nitrogen requirement for protein (fmol cell</italic><sup><italic>−1</italic></sup><italic>)</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>Nitrogen requirement for DNA (fmol cell</italic><sup><italic>−1</italic></sup><italic>)</italic></th><th align="char" valign="top" char="±" charoff="50"><italic>Nitrogen requirement for protein+DNA (fmol cell</italic><sup><italic>−1</italic></sup><italic>)</italic></th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Average open ocean</td><td align="char" valign="top" char="±" charoff="50">0.0488±0.0008</td><td align="char" valign="top" char="±" charoff="50">2.01±0.01</td><td align="char" valign="top" char="±" charoff="50">34.0±0.2</td><td align="char" valign="top" char="±" charoff="50">14.833±0.145</td><td align="char" valign="top" char="±" charoff="50">0.3377±0.0002</td><td align="char" valign="top" char="±" charoff="50">113.03±0.04</td><td align="char" valign="top" char="±" charoff="50">34.443±0.337</td><td align="char" valign="top" char="±" charoff="50">4.802±0.029</td><td align="char" valign="top" char="±" charoff="50">39.245±0.346</td></tr><tr><td align="left" valign="top" charoff="50">Open-ocean high G+C</td><td align="char" valign="top" char="±" charoff="50">0.0495±0.0007</td><td align="char" valign="top" char="±" charoff="50">2.00±0.01</td><td align="char" valign="top" char="±" charoff="50">49.9±0.2</td><td align="char" valign="top" char="±" charoff="50">14.941±0.130</td><td align="char" valign="top" char="±" charoff="50">0.3521±0.0002</td><td align="char" valign="top" char="±" charoff="50">110.62±0.03</td><td align="char" valign="top" char="±" charoff="50">35.831±0.308</td><td align="char" valign="top" char="±" charoff="50">4.898±0.036</td><td align="char" valign="top" char="±" charoff="50">40.729±0.304</td></tr><tr><td align="left" valign="top" charoff="50">Open-ocean high cell volume</td><td align="char" valign="top" char="±" charoff="50">0.0634±0.0011</td><td align="char" valign="top" char="±" charoff="50">2.00±0.01</td><td align="char" valign="top" char="±" charoff="50">34.1±0.3</td><td align="char" valign="top" char="±" charoff="50">17.282±0.180</td><td align="char" valign="top" char="±" charoff="50">0.3378±0.0003</td><td align="char" valign="top" char="±" charoff="50">113.02±0.05</td><td align="char" valign="top" char="±" charoff="50">40.138±0.425</td><td align="char" valign="top" char="±" charoff="50">4.785±0.033</td><td align="char" valign="top" char="±" charoff="50">44.923±0.435</td></tr><tr><td align="left" valign="top" charoff="50">Open-ocean large genome size</td><td align="char" valign="top" char="±" charoff="50">0.0491±0.0008</td><td align="char" valign="top" char="±" charoff="50">3.90±0.01</td><td align="char" valign="top" char="±" charoff="50">34.1±0.2</td><td align="char" valign="top" char="±" charoff="50">14.875±0.130</td><td align="char" valign="top" char="±" charoff="50">0.3377±0.0002</td><td align="char" valign="top" char="±" charoff="50">113.02±0.04</td><td align="char" valign="top" char="±" charoff="50">34.543±0.313</td><td align="char" valign="top" char="±" charoff="50">9.332±0.027</td><td align="char" valign="top" char="±" charoff="50">43.875±0.306</td></tr><tr><td align="left" valign="top" charoff="50">Ideal open ocean</td><td align="char" valign="top" char="±" charoff="50">0.0103±0.0002</td><td align="char" valign="top" char="±" charoff="50">2.01±0.02</td><td align="char" valign="top" char="±" charoff="50">34.1±0.3</td><td align="char" valign="top" char="±" charoff="50">5.929±0.060</td><td align="char" valign="top" char="±" charoff="50">0.3378±0.0003</td><td align="char" valign="top" char="±" charoff="50">113.02±0.05</td><td align="char" valign="top" char="±" charoff="50">13.769±0.142</td><td align="char" valign="top" char="±" charoff="50">4.796±0.044</td><td align="char" valign="top" char="±" charoff="50">18.565±0.169</td></tr><tr><td align="left" valign="top" charoff="50">‘Coastal' ocean</td><td align="char" valign="top" char="±" charoff="50">0.0635±0.0009</td><td align="char" valign="top" char="±" charoff="50">3.90±0.02</td><td align="char" valign="top" char="±" charoff="50">49.9±0.3</td><td align="char" valign="top" char="±" charoff="50">17.303±0.140</td><td align="char" valign="top" char="±" charoff="50">0.3521±0.0002</td><td align="char" valign="top" char="±" charoff="50">110.62±0.04</td><td align="char" valign="top" char="±" charoff="50">41.495±0.330</td><td align="char" valign="top" char="±" charoff="50">9.526±0.040</td><td align="char" valign="top" char="±" charoff="50">51.021±0.318</td></tr></tbody></table><table-wrap-foot><fn id="t1-fn1"><p>Abbreviations: ARSC, atoms per residue side chain; N, nitrogen.</p></fn><fn id="t1-fn2"><p>Parameters and calculations based on observed relationships and previously published data as described in Materials and methods.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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